On the Current Debate About Soil Biodiversity
Aus dem Institut für Agrarökologie
Traute-Heidi Anderson Hans-Joachim Weigel
On the current debate about soil biodiversity
Manuskript, zu finden in www.fal.de
Published in Landbauforschung Völkenrode 53(2003)4, pp. 223- 233
Braunschweig Bundesforschungsanstalt für Landwirtschaft (FAL) 2003
T.-H. Anderson and H.-J. Weigel / Landbauforschung Völkenrode 4/2003 (53):223-233 223
On the current debate about soil biodiversity
Traute-Heidi Anderson1 and Hans-Joachim Weigel1
Abstract Zusammenfassung
Extreme exploitation and maltreatment of land in a Zur gegenwärtigen Auseinandersetzung zum Thema number of countries had devastating impacts on terrestri- Bodenbiodiversität al ecosystems (i.e., loss of biodiversity of flora and fauna). Biodiversity became a political topic (UNEP, and Con- Da frühere Fälle extremen Raubbaus an Böden und vention on Biological Diversity (CBD) of the United schlechter Bewirtschaftung verheerende Auswirkungen Nations) decades ago and was recently linked to agricul- auf terrestrische Ökosysteme in einer Anzahl von Ländern tural practices in general (OECD, FAO). A survey of hatten (z. B. Verlust der Biodiversität von Flora und reports on “sustainable land use”, “soil fertility”, and Fauna), entwickelte sich der Begriff Biodiversität zu “soil biodiversity” which are published by such organiza- einem politischen Thema und wurde auch erst vor kurzem tions leave the impression that soil fertility is controlled in einen allgemeinen Zusammenhang mit landwirtschaft- by soil biodiversity. In essence this would mean that a low licher Praxis gebracht (OECD, FAO). Eine Sichtung von soil fertility occurs together with a decrease in soil biodi- Berichten über “nachhaltige Landnutzung”, “Boden- versity. Here is the point where assumptions and scientif- fruchtbarkeit” und “Bodenbiodiversität”, die durch diese ic evidence are far apart with respect to below-ground bio- Organisationen veröffentlicht wurden, vermittelt den Ein- diversity. Because the current discussion propagates soil druck, dass Bodenfruchtbarkeit durch Bodenbiodiversität biodiversity as a soil quality indicator, it seems necessary gesteuert bzw. von ihr abhängig sei. Dem Sinn nach würde to question this approach with respect to microbial biodi- dies bedeuten, dass eine geringe Bodenfruchtbarkeit die versity of soils. Biological soil functions such as the main- Folge verminderter Bodenbiodiversität sei. Diese Sicht- tenance of soil fertility are based on the concerted action weise stellt jedoch eher eine Annahme dar, die gegenwär- of soil organisms such as soil microflora and soil fauna. tig durch wissenschaftliche Belege nicht gestützt werden For both biological entities no specific soil functions can kann. Da in der zur Zeit anhaltenden Diskussion über be assigned to species diversity per se. Since organic mat- “Bodenbiodiversität” der Begriff schon als Bodenqua- ter turnover and nutrient turnover are mainly dependent litäts-Indikator vorgeschlagen wird, erscheint es aus on the activity of the soil microbial biomass (bacteria and mikrobiologischer Sicht angebracht, diesen Ansatz zu fungi), the present paper concentrates on this biological hinterfragen. soil fraction. Biologische Bodenfunktionen, wie der Erhalt der An attempt will be made to give an overview of the sci- Bodenfruchtbarkeit, basieren auf der Wechselwirkung entific background of soil microbial biodiversity. Interde- zwischen Bodenorganismen wie der Bodenmikroflora und pendencies between the abiotic and biotic components der Bodenfauna. Für beide biologischen Einheiten kann will be described, together with the relationship between keine bestimmte Bodenfunktion genannt werden, die in above-ground and below-ground biodiversity. irgendeiner Weise mit Artenvielfalt per se in Zusammen- hang zu bringen wäre. Da der Umsatz organischer Sub- Keywords: soil microbial biodiversity, eco-physiological stanz und der Umsatz von Nährstoffen in der Hauptsache quotients, fungal:bacterial ratio, Cmic/Corg ratio, qCO2 von der Aktivität der mikrobiellen Biomasse des Bodens (Bakterien und Pilze) abhängig ist, konzentrieren sich die Ausführungen auf diese biologische Bodenfraktion. Es wird versucht, Hintergrundwissen zum Thema mikrobielle Biodiversität von Böden aus der einschlägi- gen Literatur zusammenzustellen. Wechselwirkungen zwischen abiotischen und biotischen Komponenten von Böden finden ebenso Berücksichtigung wie die Bezie- hung zwischen der oberirdischen und unterirdischen Bio- diversität.
Schlüsselworte: mikrobielle Bodenbiodiversität, ökophy- 1 Institute of Agroecology, Federal Agricultural Research Centre (FAL), siologische Quotienten, Pilz:Bakterien-Verhältnis, Bundesallee 50, 38116 Braunschweig/Germany Cmic/Corg-Verhältnis, qCO2 224
1 Introduction identify isolated organisms. This does not speak for a quick routine lab procedure. Since intensification of agricultural production was The last decade has produced a great number of scien- identified as one of the major factors of soil destruction tific papers, mainly reviews, reflections or assumptions on and loss of biodiversity per se, international organizations soil microbial biodiversity and ecosystem function (i.e. (United Nations Conference on the Human Environment Turco et al., 1994; Beare et al., 1995; Kennedy and Smith, (UNEP), 1972; Convention on Biological Diversity 1995; Bengtsson, 1996, 1998; Wolters, (ed.), 1997; Giller (CBD)1992; OECD, 2001) have provided the necessary et al., 1997; Sparling, 1997; Bowman, 1998; Andrén and platform and have worked out strategies on how to pro- Balandreau, 1999; Wardle et al., 1999a,b). Taken together, ceed in order to introduce and keep “sustainable land use” the majority of information given here does not allow the a political issue. In discussing ways how to protect terres- conclusion to be drawn that soil biodiversity regulates soil trial ecosystems with their natural resources and biota fertility. On the contrary, the majority of authors advocate against irreversible losses, they have called upon their an opinion which was provocatively expressed by Bengts- members to contribute indicators which would be applica- son (1996) “there is no (direct) mechanistic relationship ble to many countries and would be helpful to policy mak- between diversity and ecosystem function. To think that ers for law enforcement. The following are excerpts of a one single number - species richness or a diversity index paper held at the OECD Expert Meeting on Soil Erosion - can capture the complex relationships between many and Soil Biodiversity Indicators, Rome, March 2003. species and the functional roles of these interactions is With respect to indicators for agriculture, “soil (micro- ..naive .. and negates most ecological research since the bial) biodiversity” is generally linked to “soil fertility” 1960s”. (FAO, 2001). Here assumptions and scientific evidence do The objective of this paper is to give a short overview of not agree. It is difficult to trace the first appearance of this the scientific information on soil microbial diversity. The combination of “soil biodiversity - soil fertility”. With intention is to point out the weakness of “soil biodiversi- respect to the impacts of agricultural management on ty” as an indicator of soil functions, particularly whenev- soils, attention has focused since the outset on identifying er a link between soil fertility and microbial biodiversity possible bio-indicators, specifically also microbiological is attempted. Since nutrient turnover for plant growth is a bio-indicators which are suitable for defining “soil quali- key function of the soil microbial decomposer communi- ty” or “soil health” (Lynch and Elliott, 1997; Dighton, ty, the present paper concentrates on this biological frac- 1997; Doran and Safley, 1997; Elliott, 1997). The defini- tion. Alternative microbial indicators for soil monitoring tions given for these two terms are actually interchange- purposes are proposed. able, whereby “soil health” comprises more the biological components of soils, i.e. “ the ability of a soil to perform 2 Species richness of soil microorganisms and ecosys- functions that are required for the biological components tem development of an ecosystem...” (Dick, 1997). Pankhurst (1997) in his review assessed the possible link between soil biodiversi- Not every natural soil ecosystem contains the same ty, soil functional processes and soil health while Altieri number of taxonomic entities. Traditionally ecologists (1999) takes a very isolated position in that he indeed sees determine the degree of species richness or diversity by a relationship between soil biodiversity and soil fertility simply counting all species in an area (or sample) of inter- with respect to crop production management. Since one est. By weighting the relative abundance of one species to functional process of the microbial community is the the total number of species, a qualitative index can be turnover of nutrients and therewith the maintenance of obtained which can differentiate between rare and domi- “soil fertility,” the pressure to aggregate viewpoints may nant species (Krebs, 1985). This information can be of have produced this oversimplification: soil biodiversity ecological significance. Microbial ecologists have adopt- predicts soil fertility. ed this procedure when trying to quantify below-ground Except for extreme soil conditions - such as deserts - biodiversity. It is an accepted ecological concept that the soil harbors the most diverse biotic communities on earth. set of environmental conditions shapes the degree of According to Hawksworth and Mound (1991), up until species richness which an ecosystem can sustain. The now only a total of 70.000 species of bacteria and fungi development from a simple to a diverse system is dynam- have been described, while an assumed 1.530.000 species ic. According to Odum (1969), there is an increase in remain undiscovered. This would mean that not more than species diversity, concurrent to the succession of an 5 % of microbes could potentially be identified. But even ecosystem from developmental stages to maturity, which this is impossible since classical cultural methods are time can, as the system ages, decrease again. consuming and for statistical treatment of species number With respect to soil microorganisms, the organic extra- and dominance estimations replicate soil analyses should cellular metabolites become important. Since the be done (Domsch, 1960). After all, experts are needed to microflora is dependent on products from the primary pro- T.-H. Anderson and H.-J. Weigel / Landbauforschung Völkenrode 4/2003 (53):223-233 225
ducer, it is a logical consequence to ask if a possible link to draw a final judgement (see also recent review by War- exists between above-ground and below-ground biodiver- dle and van der Putten, 2002). sity. As could be expected, this has opened a new discus- Spatial heterogeneity (number of habitats or niches per sion (Wardle and Giller, 1996; Bardgett et al., 1998; Wall unit area) is another physical factor for diversity gradients and Moore, 1999; Hooper et al., 2000; Adams and Wall, (Risser, 1995). In a recent review, Ettema and Wardle 2000; Wolters et al., 2000) on an old topic. Early publica- (2002) delivered theoretical arguments for the causes of tions trace the appearance of microorganisms to specific subsequent spatial variability of organism distribution and plant residues (Domsch and Gams, 1968; Martyniuk and how this may influence the plant community. A system is Wagner, 1978) and an increase in taxonomic fungal diver- structured by species interactions with their habitat and by sity with increasing resource heterogeneity (Zak and Viss- species to species interactions which leads to higher er, 1996 (sensu Gochenhaur, 1975)). New experimental species diversity. Waid (1999) cites two main modes of reports are scarce. organismal interactions: direct interactions, such as troph- In an experiment where soil was primed with different ic, symbiotic, parasitic, or predatory types of interaction, C-sources, an increase in in situ catabolic potential of the and the indirect interactions, where organisms change the microflora was found (Degens, 1998a), while Stephan et environment enabling others to emerge. He revived the al. (2000) determined the catabolic diversity of culturable old term metabiosis to describe such indirect interactions. soil bacteria (BIOLOG method) which increased with the Soil ecology of the past has contributed a great wealth of number of plant species in a grassland ecosystem. How- knowledge on direct interactions. Particularly early stud- ever, in both of these studies indirect methods are applied ies on pioneer organisms and successional stages of and it remains unclear whether the observed increased organismal appearance during organic matter degradation catabolic potential or diversity was due to the appearance (Swift, et al., 1979), in addition to the studies on the sig- of new organisms or if the old community stayed nificance of food webs in structuring soil communities unchanged but reactivated catabolic potentials. Brodie et (Lavelle, 1995, Lavelle et al. 1997; Duffy, 2002; Dunne et al. (2002), studying a grassland transect (from 25 to 6 al., 2002), have given some insight on how communities plant species), did not see a relationship between plant evolve. On the other hand, the concept of indirect interac- species diversity and bacterial diversity when using a tions has not extended over the borders of theoretical ecol- molecular approach, a bacterial community fingerprinting ogy with only little experimental work so far. It must be technique (TRFLP analysis). The highest plant diversity assumed, however, that metabiosis interrelationships had the lowest bacterial diversity, bacterial numbers, “whereby organisms must modify their environment microbial biomass-C and catabolic potentials (BIOLOG). before others are able to live and evolve” (Waid, 1999) Unfortunately, the soil pH was lowest (3.9) in the plot must first occur before direct interactions can take place. with the highest plant diversity and highest (6.3) in the Further, under conditions of environmental (i.e., climat- plot with the lowest plant diversity. Here a pH effect was ic) stability, the highest degree of diversity can be expect- measured and not the effect of the number of plant species ed. on the microbial community since it has been shown that The question of ecological organization of communities soil pH controls the microbial community and that bacte- has engaged the ecological literature for a long time. The ria will decrease at low pH (Anderson, 1998; Blago- majority of authors agree that it is not each individual datskaya and Anderson, 1998, 1999). This indicates that species in a community that has the same impact on its soil physico-chemical factors are the primary determi- habitat, but that a community can be differentiated into nants in establishing microbial communities, and that fur- “drivers and passengers” (Peterson et al., 1998, Risser, ther diversification may then be controlled by the degree 1995). A “driver” would have a strong ecological func- of available heterogeneous extracellular metabolites or tion, which in microbiological studies is similar to the organic substrates, respectively. However, it still remains term “keystone” species (Beare et al., 1995). This is inde- open whether such a diversification must be understood as pendent of species richness. The general ecological an increase in the number of species or if heterogeneous notion until now has been that of an undirected develop- plant products induce diversification of catabolic func- ment of community differentiation into species richness. tions or both. These two alternatives were highlighted in This development is rather stochastic. Given the possibil- the work of Broughton and Gross (2000). The authors did ity of two similar habitats, will the same microbial spectra not find a relationship between plant species richness and evolve in both? No prediction can be made here (Swift, microbial species richness as indicated by fatty acid 1984). Ecosystem theory discusses, however, an underly- methyl ester (FAME) profiles, however, they found an ing principle of development of a system to higher effi- increase in catabolic potentials (BIOLOG). This aspect of ciency in conserving energy (Odum, 1969; Reynolds, plant species richness and microbial species richness 2002). All this shows how difficult and inexact the term needs further exploration since it is a fundamental ecolog- (microbial) diversity can be. We do not know what kind of ical question and experimental evidence is still too scarce species richness can be expected in a habitat. A summary 226
Ecosystem development (2nd law of thermodynamics)
S c t l ) i a ) m b H a p e a i r l above-ground biodiversity t i , a e t e y it , r y e.g., mixed forests t n e u i t u n e x r multi-species grassland v e e n i p r t e o s . g n e g o heterogeneous organic material m . r h c e e i e t n ( high organic matter content nt e s r i h o a s l s l t e a c i ta o n t i nutrient status n e a b a d g p h i o t S f i d o species o e r n e P interactions s b m direct u n ( indirect such as trophic, by metabiosis parasitic, symbiotic, predatory
Ecosystems are never alike! Microbial diversity cannot be predicted!
Fig. 1: Main factors which determine natural microbial diversity. These principles apply as well to man-manipulated soil systems. A threshold value of soil microbial diversity at the species level cannot be established. of the points made here is given with a schematic soil texture, soil pH and as well to the capacity to retain overview in Figure 1. nutrients and moisture. These are key properties of soils for the development of above-ground vegetation and main 3 Natural versus man-made soil fertility - links to properties which are - among others - connected with soil microbial soil biodiversity fertility. These properties are not equally distributed in nature, and from the practical viewpoint of an agronomist Because of the unpredictability of species richness with respect to field-crop production and potential crop development and the current belief that species richness is yield, gradients of low to extremely high soil fertility not linked to known functions of ecosystems, but rather would be identified as seen with chernozems. The most that single organisms or groups of organisms occupy func- intriguing fact from an ecological point of view is, how- tions, the majority of papers propagate the necessity to ever, that the most naturally “fertile” soils carry the least identify “keystone processes”, “keystone species” or species richness of plants, animals and most probably of “keystone groups” of organisms (e.g. Domsch, 1968; microflora and fauna as well (Marrs, 1993; Risser, 1995). Hawksworth and Mound, 1991; Walker, 1992; Beare et That means, the assumptions commonly expressed that al., 1995; Risser, 1995; Giller et al., 1997; Jones and Brad- soil biodiversity would be an indicator of agricultural soil ford, 2001; Tebbe et al., 2002) which drive ecosystems. fertility or vice versa is diametrically opposed to obser- One prominent keystone process is the development or vations made in natural environments. maintenance of “soil fertility”. The topic of protecting More recent investigations on semi-natural plant pro- soils against loss of soil fertility caused by agricultural duction show an increase in net primary productivity intensification has engaged the international policy advi- (NPP) with increasing plant species richness in grassland sory boards for many years (FAO, CBD). Since plant ecosystems (Tilman et al., 1996, 1997, 2002; Hector et al., (crop) production is dependent on soil fertility, the main 1999, 2002; Bullock, et al., 2001; Knops et al., 2001). Par- concern is that losses of organisms which are controlling ticularly from the work of Hector et al., (1999) where agents of soil fertility could lead to losses in crop yield. eight European countries were involved in the study, it can The natural intrinsic soil fertility and knowledge about the be assumed that this observed increase in phytomass with natural soil (microbial) biota and its reaction to degrees of increasing plant species richness was independent of the fertility or environmental stress is appropriate to be used underlying natural soil fertility of those sites. Two very as a baseline (Domsch, 1977; Domsch et al., 1983). It is important aspects emerged from these studies: the obvious that natural soil fertility differs due to pedogene- increased productivity lead to a higher uptake by the sis (soil-building processes), which lead to the origin of plants of available soil nitrogen but did not lead to a faster T.-H. Anderson and H.-J. Weigel / Landbauforschung Völkenrode 4/2003 (53):223-233 227
Fig. 2: Schematic view of the biotic components which are assembled under the term “soil biodiversity”. The need to dif- ferentiate! Dark grey sections show the decomposer (called microbial biomass of fungi and bacteria) which are the main actors of organic matter degradation and nutrient turnover together with the soil fauna which physically trans- form litter to smaller pieces for better attacks by microbes. Both activities are contributions for a higher soil fertili- ty. A high nutrient status (high soil fertility) will positively affect the decomposer community (the bacteria and fungi) while other groups of organisms (white fields) will be suppressed. rate of litter degradation (Tilman et al., 1996; Knops et al., determined between soil microbial biomass and soil 2001; Catovsky et al., 2002). Since the heterotrophic organic carbon (Anderson and Domsch, 1980) in agricul- microflora competes for the same mineral nutrients as tural and forest soils (Anderson and Domsch, 1989, 1992). plants do, the inorganic form of N, such as nitrate, may Since the microbial biomass is a potential source for plant be less available for this group of microbes under such nutrients (Anderson and Domsch, 1980; Marumoto et al., conditions. Low nitrate availability and low soil fertility, 1982a,b; Brookes et al., 1984) a high level of microbial however, promotes microbial specialists, the free-living biomass is an indicator of a highly fertile soil. As pointed nitrogen fixing organisms (bacteria), and rhizosphere out above, increasing plant species diversity resulted in organisms of leguminous plants such as rhizobia (see higher litter production. With time such systems should review by Brockwell et al., 1995) and a special form of also produce a higher level of soil organic matter. Recent rhizosphere organisms, the arbuscular mycorrhizal fungi reports seem to verify this relationship between plant (AMF) (van der Heijden, et al., 1998a,b). species richness and increases of microbial biomass The bulk soil harbors the main important heterotrophic (Broughton and Gross, 2000; Bardgett and Shine, 1999; microbial community responsible for organic matter Spehn, et al., 2000). Based on recent experimental evi- decomposition, nutrient cycling and soil building process- dence one can assume, however that soils with higher es (structuring soil by extra-polysaccharide production). microbial biomass levels will also carry a greater species These functions of a microbial community are related to diversity. Yan et al., (2000) described an increase in possi- soil fertility by the soil biologist, while the agronomist ble species diversity (indirectly measured by CLPP often includes the other plant promoting “services” as method using BIOLOG) up to a soil organic carbon con- well which are lumped under the label soil fertility (e.g., tent of 1.76 %. Beyond this value catabolic potentials rhizosphere effects, control of pathogens, etc.). As point- remained constant. Also Øvreås and Torsvik (1998) ed out above, heterotrophic organisms need nutrients (N, showed for all test parameters applied (BIOLOG and P, K) for growth and decomposition activity while nutrient molecular methods, e.g., amplified rDNA restriction poor environments will promote the specialist. This is analysis (ARDRA)) a higher bacterial species richness in illustrated in Figure 2. In other words, normal agricultural an organic soil with 25 % Corg as compared to a soil with practices counteract processes of species diversity devel- 4.5 % Corg. Also, Degens et al. (2000) found a relationship opment which happen in natural ecosystems. between catabolic potential of the microbial communities In natural soil systems the heterotrophic microbial com- to different % of organic C by studying 22 soils of differ- munity is not evenly distributed. A linear relationship was ent texture. There was a decline in catabolic diversity in 228
Table 1: Field Comparison of calculated Cmic-to-Corg* values taken from Fig. 3 of dif- ferent agricultural managed plots and forest sites. 1000 2 900 R = 0.7884 Type of soil Cmic in Corg 800 land use conditions (%) y = 311.33x - 28.6 700 600 Field soil Monoculture NPK 2.36 -1 500 FYM 2.60 400 µg g µg monoculture GM+S 4.00 300 crop rotation 200 n= 135 Crop Rotation NPK 2.90 FYM 2.50
Microbial biomass carbon 100 Ap horizon GM+S 2.71 0 Forest 0 1 2 3 MonoBeech pH > 6.0 2.30 [%] Soil organic carbon MonoSpruce pH > 6.0 2.00
Mixed-Beech-Oak pH > 7.0 2.70 Forest pH >6.0 * Calculated % Cmic in Corg (Field) are from a great number of long-term European field plots. They could be used as 3500 threshold values for a particular soil management (Ander- son and Domsch, 1989). FYM = farmyard manure; R2 = 0.6734 3000 GM+S= green manure + straw. y = 208.92x + 165.3 2500 what natural stressors can produce. Early thorough inves- 2000 tigations of naturally occurring stresses and their impact soil
-1 on soil microorganisms (e.g., temperature, pH, O2 ten- 1500 sions, desiccation, physical disturbance, nutrient supply) µg g 1000 beech/beech-oak demonstrate that more than 50 % of organisms or meta- n=150 bolic activity can be lost, which can be considered as a 500 Ah horizon normal natural phenomenon (Table 2). Depending on the
Microbial carbon biomass 0 mean doubling time of a community, time must elapse 0 5 10 15 until a community has reached the initial level of organ- isms again. In the majority of stress cases explored, the [%] Soil organic carbon microorganisms recovered within less than 30 days. Sim- ilar observations were made in pesticide-side effect stud- ies where 89 % of all cases (60 pesticides) showed a Fig. 3: recovery time of less than 30 days (Domsch, 1977; Relationship between soil organic carbon and microbial biomass carbon in agricultural and forest soils. The plots show data points from either Domsch et al., 1983). The monitoring of time is an impor- long-term (>15 yrs) monocultures or crop rotations or pure beech stands Table 2: and mixed beech/oak stands. Data points above the regression lines are Natural stress impacts on populations and metabolic processes of soil from crop rotations or mixed forest stands while data points below the microbial communities (Data extracted from Domsch et al., 1983). regression lines are from monocultures or pure beech stands. This indi- cates that diversity of the above-ground phytomass will positively affect the level of microbial biomass (data extracted from Anderson and Dom- Cause Organisms/ Process Depression (%) sch, 1989; Anderson, 2003). soils where carbon is lost by management. Figure 3 and Compaction Nitrification 50 - 75 Table 1 give examples of the relationship between soil Drainage Denitrification 66 - 93 organic carbon and microbial carbon. The aspect, howev- Flooding Ammonification 98 Flooding (aerobic) bacteria 48 - 91 er, of the relationship between soil carbon content, level Flooding Actinomycetes 76 - 98 of microbial biomass together with studies of species rich- Reduced O2 Fungi (growth) up to 80 ness has found little attention so far, but seems vital in Reduced O2 Bacteria 90 - 100 identifying indicators of species richness. Reduced O2 Nitrification 28 - 70 If impacts on the microflora by agricultural manage- Protozoa Bacteria 66 Collembola Fungi 70 - 95 ment should be assessed, it is necessary to take a look T.-H. Anderson and H.-J. Weigel / Landbauforschung Völkenrode 4/2003 (53):223-233 229
tant criterion for assessment of the resilience of a com- ty to degrade litter is a vital property of the heterotrophic munity and its ability to recover. The resilience in soil microbial community. response to a natural impact could serve as a yardstick when assessing negative anthropogenic impacts (Domsch, 4 Soil microbial indicators which are sensible for mon- 1977; Domsch et al., 1983) (Figure 4). itoring sustainable land use
Natural stresses The examined literature does not allow the conclusion Cases of natural stresses to be drawn that under conventional agricultural practices 12 10 in the temperate regions (except for heavy metal contam- 8 inations or soil erosion cases) soil fertility is lost. Changes 6 observed in the microbial community under necessary 4 agricultural practices (tillage, plowing, pesticide treat- 2 0 ment, fertilizing) were transient and could not be related 10 20 30 40 50 60 70 >70 to decreased activities of the heterotrophic soil communi- Recovery time (days) ty to degrade organic matter, the key function for nutrient Fig. 4: cycling. Agriculturally managed land cannot evolve into a Example of recovery time of soil microorganisms after impacts of dif- species-rich habitat compared to natural systems; its func- ferent types of natural stress. Compare Table 2 (according to Domsch et tion to produce crop yield counteracts a development to al., 1983). higher species richness in a system. Vandermeer et al., Agricultural land should yield enough crops for the (1998) demonstrated this by comparing different types of world`s food demand and yield is the source of income for land use, from unmanaged systems to low or middle inten- the farmer. Even if all the propositions would be met sity managed systems up to degrees of high intensity such which are cited in the agro-ecological test KUL (VDLU- as plantations and orchards, intensive cereal or vegetable FA, 1998) for sustainable land use, agricultural soils will production. Along with land use intensification, a still be overloaded with nutrients which are necessary for decrease in the overall species diversity was observed. obtaining an optimal crop yield. Since plants (crops) are However, because of the functional redundancy of het- harvested and not returned to the soil, it is necessary to erotrophic abilities of the microflora nutrient turnover will supply the soil with available nutrients. Still soil C loss be secured in every type of land use. can be substantial in the long run (Saggar et al., 2001). This may be a very narrow and utilitarian view to focus Even under the most careful mechanical soil treatment, only on the function “soil fertility” or other functions there will be disturbances of microbial communities which “serve” man. Although organisms are complemen- (Domsch, 1986). The otherwise self-regulating soil sys- tary - if one species is lost, another species takes over tem is continuously interrupted by these activities. This (Griffiths et al., 2001) -, it cannot be ruled out that lost again means, below-ground soil biodiversity in agricul- species had genetically fixed traits for functions which we tural soils can never be attained to such an extent as have not yet identified. Sustainable land use should be under natural conditions. Using an indirect test by propagated for protecting the intrinsic soil biodiversity in determining the functional diversity of microbial com- the light of a possible changing world (global change) munities of uncultivated and cultivated soils, community (Weigel, 1997) and as stated in the CBD “to meet the level physiological profiles (CLPP) were greater in uncul- needs and aspirations of present and future generations”. tivated soils (BIOLOG test, Yan et al. 2000). The high Microbiological indicators of biodiversity should meet load of nutrients raises a problem, for instance, when the following criteria according to the OECD Joint Work- measures of agricultural extensification are to be carried ing Party on Agriculture and Environment (JWP). They out by turning agricultural land into floristically rich nat- should be: policy-relevant, analytically sound, measura- ural sites; the removal of surplus nutrients can take many ble, and easy to interpret. This would exclude for the time decades (Gough and Marrs, 1990). It can be stated, how- being descriptive methods (non-quantitative) such as new ever, that in conventionally managed soils, microbial molecular methods (White and Mcnaughton (1997). Here, species richness also is great. A seven-year study by War- more experience is needed to understand limitations of the dle et al., (1999b) did not indicate loss of microbial activ- methods employed, and quantification is a must for com- ity due to agricultural intensification. Also, experimental parative purposes and statistical treatments. The same approaches in which soil biodiversity was diminished or would apply for the biochemical phospholipid fatty acid changed did not show a decrease in decomposition rate or (PLFA) method which discriminates between bacteria and heterotrophic activity (Andrén et al., 1995; Degens, fungi (White, 1983). Both approaches are alluring since 1998b; Griffiths et al., 2001). Andrén et al. (1995) discuss they will ultimately eventually give a direct insight into the role of functional redundancy (functionally equivalent species diversity (community structure). In addition to the species) particular with respect to degradation. The abili- obstacle mentioned above, the results obtained cannot be 230
related to a function per se, since we do not know if the molecular or fatty acid signals obtained belong to organ- isms which are engaged in activities under study or if they 100 include dormant organisms as well. Organisms can sur- vive over decades in a resting stage! 80 Ecophysiological indicators are an alternative to over- 60 come these current limitations. The advantage is that these Bacteria -output indicators integrate abiotic and biotic components. One 2 40 such indicator is the metabolic quotient, qCO2, (CO2 pro- Fungi duction per unit cell mass and time) which was extrapo- 20
lated from in vitro studies on the microbial biomass in soil CO [%] (Anderson and Domsch, 1985a,b; Anderson 1994) and 0 which links respiratory activity (basal respiration) to the (total respiration = 100%) size of the biomass. Negative environmental changes will 0.0 2.0 4.0 6.0 8.0 be reflected in this quotient (Anderson and Domsch, 1993). It also satisfies the concept of comparing a meas- Soil pH ured effect with the reaction under “normal,” undisturbed Fig. 5: conditions. The CO2 release from basal respiration also reflects to a certain degree the maintenance carbon The respiratory response of fungi and bacteria in relation to soil pH. Per- cent of respiratory contributions by bacteria decreases with decreasing requirement of the cells. To adapt to adverse changes the soil pH. Forest soils (Ah) of Lower Saxony, Germany, n=60 (Anderson, microbial community will have a higher maintenance 2005, in print). requirement, expressed as qCO2. This quotient has been accepted by the scientific community and a large body of large body of scientific background information on these experimental results is available. The same applies to the quotients. Cmic/Corg ratio. It relates microbial biomass (Cmic) to total soil organic carbon (Corg). As pointed out above, this rela- 5 Concluding remarks tionship between microbial biomass and soil carbon is not sporadic but very stable. It reflects the availability of the Possible driving forces of soil microbial diversity which soil carbon for the microbes. In the temperate zone the could be considered for sustainable land use or land con- Cmic/Corg ratio is about 2.5 % of total organic carbon servation were sought in the body of scientific literature. (Table 1). For instance, changes in the organic matter In addition, an attempt was made to place the term “soil quality will be reflected in this ratio. If a community is fertility” into the correct perspective at the level of soil stressed a high qCO2 is expected which must, should the microbial biomass and not at the intrinsically existing bio- stress remain, lead to a lower Cmic/Corg ratio (Anderson, diversity of a microbial community. 1998, Anderson and Domsch, 1989). These two ratios together are useful for monitoring soil systems (Turco et The following inter-relationships were identified: al, 1994; Sparling, 1997; Dilly and Blume, 1998; Staddon 1.With respect to a higher diversity of plant species (long- et al., 1999; Anderson, 2003). The fungal/bacterial respi- term) ratory ratio (Anderson and Domsch, 1975) is an addition- a. by production of more phytomass al physiological parameter. It can differentiate between b.a higher level of organic matter is attained with time the respiratory activity of bacteria and fungi by selective- c. which will contribute to a more heterogenous supply of ly inhibiting the respiration with antibiotics. Normally organic matter below-ground, and thus may influence agricultural soils have a respiratory ratio where fungal res- diversification of the microbial community (Figure 1) piration is 80 % and bacterial respiration is 20 % of total (here research is still needed). respiration. This ratio changes if one microbial fraction is 2.The level of organic carbon will be a driving force for impared or lost. In this respect this quotient also reflects microbial biomass development (Figure 3). changes in diversity. For instance, a decrease in bacterial 3.A high microbial biomass level under agricultural con- respiratory activity with decreasing soil pH (Anderson, ditions would be an indicator of high soil fertility and 1998; Blagodatskaya and Anderson, 1998, 1999) was 4.first results indicate a relationship between species or identified (Figure 5). functional diversity to high biomass levels (here These three microbial quotients are relatively easy to research is still needed). measure, are reproducible, understandable, and, with 5.Soil pH is one of the main abiotic factors controlling exception of the initial costs for the necessary equipment diversification. Under neutral pH the highest fungal and are relatively inexpensive. They are applicable across all bacterial diversity can be expected, with decreasing pH countries. An additional advantage is that there exists a bacterial activity will decrease (Figure 5). T.-H. Anderson and H.-J. Weigel / Landbauforschung Völkenrode 4/2003 (53):223-233 231
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